Thursday, June 22, 2017

At the Speed of Life

Twenty years ago, Mike
Kinnison and I started thinking seriously about evolutionary rates. Over
the years since, we – with many collaborators – have assembled a database of
evolutionary rates that has been used by ourselves and many others for various
purposes. We are currently in the midst a big new push to add additional
studies to the database and we would like YOUR help. In short, if you have
studied rates of phenotypic change in contemporary populations, we think it
would be cool to have your study in the database. Information on how to
participate is at the end of this blog post that traces the history of the
database.

The whole thing accelerated for us in 1997, when Mike Kinnison
and I were graduate students sitting in adjacent desks at the School of
Fisheries in the University of Washington. At the suggestion of our prescient
supervisor, Tom Quinn, we
were both studying salmon introduced to new environments with an eye to how
rapidly they might be evolving. Mike was working on chinook salmon introduced
into New Zealand and I was studying sockeye salmon introduced into Lake
Washington. And we were finding plenty of evidence that, in both cases,
substantial evolutionary change had occurred since the introductions.

Mike Kinnison checking on his chinook salmon in the mid 1990s, New Zealand.

Me with a sockeye salmon the mid 1990s - here in Alaska.

In the midst of our work in 1997, two high profile papers
were published that documented similarly rapid phenotypic changes in populations
experimentally introduced into new environments – guppies in Trinidad (Reznick et al. –
Science) and Anolis lizards in the Caribbean (Losos
et al. – Nature). (These came to our attention via a commentary
in TREE written by Erik Svensson.) A few papers showing pretty much the same
thing had come out previously, but these two new papers were different in one
important respect – both formally quantified evolutionary rates for their
studies and compared them to evolutionary rates reported in the fossil record. For
both guppies and lizards, evolution in contemporary time was several orders of
magnitude more rapid than evolution typically observed in the fossil record,
which brought a lot of scientific and media attention to how rapid ongoing evolution
seemed to be. In short, instead of the “we see nothing of these slow changes in
progress until the hand of time has marked the long lapse of ages” wisdom received
from Darwin, a more correct conclusion might be “we can often see rapid changes
in progress even though the hand of time has barely moved.”

“Wow, that’s pretty cool”, Mike and I thought, “let’s calculate
rates of evolution in our own study systems and see how fast they are – which was
when the whole thing began to complexify. As we delved into the details of how
evolutionary rates were calculated and interpreted, it became clear that many
ambiguities, uncertainties, caveats, and subtleties were involved. This caution
seemed to us important enough – and certainly relevant enough to our own work –
to warrant writing something about it, which we duly published in 1998 as a
short note (Taking
Time with Microevolution) in TREE.

My first publication with Mike. When I asked him what his middle initial stood for, he insisted it was "Michael The Kinnison."

After publishing this note, Mike and I continued to work on
the problem and it became abundantly clear that it warranted a full-length treatment
about how best to estimate evolutionary rates and that also calculated and
reported those rates for a bunch of studies beyond the only two that (at that
time) had done so for contemporary populations. The problem, of course, was
finding the time to write the paper while we were both in the throes of
finishing our PhDs and starting our postdocs, which were on quite different topics.

Fortunately, right about this time, I was invited to work on
a project in southern France where data collection took place mainly by camera
recordings. Thus, once the experiment was set up, I had some extra time to
perhaps write something else up. Although I certainly had tons of things to
write up, the different venue provided mental freedom enough to say, “why not
try to blast out this evolutionary rate paper.” So I very rapidly wrote up a
first draft that Mike and I then edited and – without much expectation –
submitted it to Evolution as a Perspective. This submission was a bit of a
stretch, or at least leap of faith (or hope), for Mike and I because – at this
point – neither of us had published anything in an evolutionary journal (instead
only in fish journals), nor had we really had much feedback from real
evolutionary biologists (although we did get good comments from the Huey/Kingsolver
lab meetings).

Lo and behold, and somewhat to our surprise, Evolution was
happy to publish the paper: The
Pace of Modern Life: Measure Rates of Contemporary Microevolution. In the
immediate aftermath, or really lack thereof, not much happened – nor had we
expected it to. In fact, we kind of viewed the paper as our own little curiosity
project that helped us to think more deeply about our own empirical work. We
guessed it might be a bit interesting to some few other researchers but
probably of little practical use or importance to most. So, once published, we continued
our progress toward other topics.

Database version 1.0 - from Hendry and Kinnison (1999).

Then – out of the blue – came an invitation from a journal
(Genetica), we didn’t know much – if anything – about, to edit a special issue
on contemporary evolution. Being quite green postdocs who had never received such
an invitation, we immediately agreed. (Nowadays, of course, the many predatory
journals are constantly inviting even inexperienced, as we were at the time, people
to edit special issues.) Importantly, we decided to invite every famous
evolutionary biologist that we knew of (but none of which we really knew
personally) who might contribute moderately relevant papers: Grant, Reznick, Losos, Sinervo,
Lande, Arnold, Riechert, Wade, Kingsolver, Gingerich, Magurran, Bell, Merila, Raymond,
Smith, etc. Remarkably, nearly all of them agreed, something that still
amazes me today – and, in fact, which I doubt would occur today.

In our invitations, we took a strategy which I now adopt in
nearly every special issue that I edit – and
there have been a lot of them: invite the best people, give them the
general topic (in this case, Microevolution:
rate, pattern, and process), and tell them they can write specifically
about whatever they want to write about in that general area. This strategy really
is the best way to make sure you get great people and great topics – although
the cleverness of it was not something we knew in advance. The only specific
additional request we gave was that, if they were reporting phenotypic changes
over relatively short time frames (several hundred years or fewer), they should
formally calculate and report evolutionary rates in accordance with our
suggestions from the earlier Evolution paper.

The main paper that Mike and I contributed to the Genetica special issue was a follow up
of our original Pace of Life paper, wherein we now calculated evolutionary
rates for more previous studies and formally analyzed the resulting database to
try to answer big questions about evolution. What is the distribution of
contemporary evolutionary rates and how do they compare to selection intensities?
Do different types of traits evolve at different rates? How do evolutionary
rates scale with time interval? In the end, the special issue had 30
contributions, a number of which have been very heavily cited (7 more than 100
times on Web Of Science).

Database Version 2.0 from Kinnison and Hendry (2001).

In 2002 or thereabouts, both Mike and I started faculty
positions, me at McGill and Mike at U Maine. (I had interviewed for the same
position at Maine but they chose Mike. Of course, things turned out well for the
both of us.) Earlier that year, I had given a talk on contemporary evolution in
the ASN Young Investigator Prize symposium and the editor of TREE, who had seen
the talk, asked if I wanted to write a paper on contemporary evolution for the
journal. I proposed several options, one of which was the implications of
contemporary evolution for conservation biology, which was the topic the editor
chose. However, I knew little about conservation and both Mike and I felt a bit
overwhelmed in our new jobs, so we contacted Craig Stockwell, who worked on
both contemporary evolution and conservation. This was an excellent decision as
Craig very cleverly tied the two fields together, and generated a paper (Contemporary
Evolution Meets Conservation Biology) that was quite influential, with 870
citations on Google Scholar.

Database Version 2.1 (really, the same as 2.0) from Stockwell et al. (2003).

But the actual database of rates was getting quite out of
date. Fortunately, I taught a graduate class at McGill where one of the student
task was to write a review/meta-analysis. I pitched to several students the
idea of expanding the evolutionary rate database, and Thomas Farrugia
– and undergrad at the time – was interested. So we then spent several months
adding papers to the database and reanalyzing it to follow up the Genetic paper. A great venue for
publishing this work then presented itself as Tom Smith and Louis Bernatchez
were organizing a symposium at UCLA on Evolutionary
Change in Human Altered Environments and were going to edit a special issue
in Molecular Ecology.

Me and Mike and the mid-2000s - in this case rockin the facial hair in Trinidad.

Thomas had moved on to other things by then, and so the
task fell to me to finish up the paper, which I spun into a consideration relevant
to the symposium/issue: whether or not human influences increased rates of
phenotypic change. Turns out they did and the paper (Human
Influences on Rates of Phenotypic Change in Wild Animal Populations) has
been heavily cited in that regard. A reviewer also forced me to do a quick
analysis, which I felt the database was not large enough for yet, that
considered which types of human disturbance led to the greatest rate of change.
This last topic proved to resonate with others into the future, as we will see
below.

Database Version 3.0 from Hendry et al. (2008).

A first, reviewer-insisted, analysis of rates of change associated with different types of human disturbance - from Hendry et al. (2008).

A difference this time was that we also published the
existing database online, which meant that anyone could grab it and re-analyze
it (usually with additions) to answer their own questions. As result, papers
have now come arguing that rates of change are greatest when humans act as
predators (Darimont et
al. 2009 - PNAS) but are not especially noteworthy in the case of invasive
species (Westley
et al. 2011 – Am Nat), that evolution should be possible in response to climate change (Skelly et al. 2007 - Cons Biol), and that trait evolution should have ecological consequences (Palkovacs et al. 2012). The database has also been used to examine the links
between micro- and macro-evolution (Uyeda et al. 2011 - PNAS), the pace of cultural evolution (Perreault et al. 2012 - PLoS ONE), and a wide variety of other topics.

Through the years, we have expanded the database a bit – and
fixed various errors and inconsistencies – to then re-analyze and publish
papers showing that (for example) body size does not evolve faster than other traits (Gotanda et al.
2015 - Evolution) and that rates of change are especially high in some
urban contexts (Alberti et
al. 2017 - PNAS).

Database Version 4.0 from Alberti et al. (2017).

Yet all of these analyses are still working with a database
that, while large and growing, is very incomplete. A large number of relevant studies
of phenotypic in natural populations have been published in the last 20 years
that could be added to the database but haven’t been – simply for reasons of
obscurity (to us) or time (for us). Thus, when I was asked this year to help
write the Intergovernmental Platform on Biodiversity and Ecosystem Services
(IPBES) Global
Assessment, I realized we needed to do a major database expansion and
overhaul. Hence, over the past half year or so we (especially my new student Sarah
Sanderson) have been accumulating studies, extracting data on phenotypic
changes, and adding them to the database. Although we have added many new
studies, it is clear that many more are still out there – yet they are
sometimes hard to find.

This need, then, is the impetus for this blog post – we would
like your help in finding as many relevant studies as possible. Sarah generated
a list of all studies in the database (we have some others still being
entered), which we provide here. If you study phenotypic change in contemporary
time, it would be fantastic if you could skim this list to see if your study is
included. If not, we would love it if you could contact us to tell us about
your study so that it can be included. Importantly, the database will – when reasonably
finished – be provided online for all to use, which can only increase its (and
your study’s) value to the scientific community. We hope that you will join us
in this endeavor as it has been fun and profitable for me – and it can be for
you to.

Cheers and thanks, Andrew.hendry@mcgill.ca

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Note: we are looking for studies of changes in quantitative traits (body size, morphology, phenology, etc.) over known time frames. These can come from information on the same population in different years (allochronic) or from different populations that had a common ancestor at a known time in the past (synchronic). It is also not necessary to have confirmation of the genetic basis for the change as people are also interested in plasticity - and, regardless, these aspects are coded for each study in the database.

2 comments:

Great to see the arc of it all laid out in one place! I can provide a small clarification. The invitation for the Genetica special issue didn't really come out of the blue, it came from an editor that saw a talk/title I gave at an evolution meeting with some preliminary analyses. Those preliminary analyses would eventually show up in our Kinnison and Hendry 2001 contribution to the Genetica special issue.

I still vividly remember the excitement of playing with those first rates and simulating analyses to see how various metrics behaved. It was mostly simple stuff, but I learned from that period that sometimes simple is what's really needed.

There's so much more that can be done with these rates. It's amazing how we went from starting all this thinking that studies of contemporary evolution were rare to knowing that there are more examples out there than we can ever hope to find on our own.